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Trait Hierarchy and Interactive Effects Govern Seed Fate in Rodent-Mediated Dispersal: Insights from Coat Thickness, Nutrients, and Tannins.

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Τίτλος: Trait Hierarchy and Interactive Effects Govern Seed Fate in Rodent-Mediated Dispersal: Insights from Coat Thickness, Nutrients, and Tannins.
Συγγραφείς: Liang H; Key Laboratory of Southwest China Wildlife Resources Conservation (Ministry of Education), College of Life Science, China West Normal University, Nanchong, China., Fu L; Key Laboratory of Southwest China Wildlife Resources Conservation (Ministry of Education), College of Life Science, China West Normal University, Nanchong, China., Ma F; State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China.; Office of University-Local Cooperation, China West Normal University, Nanchong, China.; College of Biology and Environmental Sciences, Jishou University, Jishou, China., Zhao K; State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China.; College of Ecology and Environment, Chengdu University of Technology, Chengdu, China., Hou Z; Key Laboratory of Southwest China Wildlife Resources Conservation (Ministry of Education), College of Life Science, China West Normal University, Nanchong, China., Guo J; Key Laboratory of Southwest China Wildlife Resources Conservation (Ministry of Education), College of Life Science, China West Normal University, Nanchong, China., Yang X; Key Laboratory of Southwest China Wildlife Resources Conservation (Ministry of Education), College of Life Science, China West Normal University, Nanchong, China.; State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China.; College of Biology and Environmental Sciences, Jishou University, Jishou, China.
Πηγή: Integrative zoology [Integr Zool] 2026 Jul; Vol. 21 (4), pp. 817-827. Date of Electronic Publication: 2026 Feb 12.
Τύπος έκδοσης: Journal Article
Γλώσσα: English
Στοιχεία περιοδικού: Publisher: Wiley Publishing Asia Pty Ltd Country of Publication: Australia NLM ID: 101492420 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1749-4877 (Electronic) Linking ISSN: 17494869 NLM ISO Abbreviation: Integr Zool Subsets: MEDLINE
Imprint Name(s): Publication: 2012-: Richmond, Vic., Australia : Wiley Publishing Asia Pty Ltd
Original Publication: 2006-2012: [Oxford, England] : Blackwell Publishing
Ιατρικοί όροι (MeSH): Tannins*/analysis , Seeds*/chemistry , Seeds*/anatomy & histology , Seed Dispersal*/physiology , Rodentia*/physiology , Feeding Behavior*, Nutrients/analysis ; Animals
Περίληψη: Seed traits play a pivotal role in shaping rodent-mediated seed dispersal, a key process driving forest regeneration. However, disentangling the independent and interactive effects of physical (coat thickness), nutritional, and chemical (tannin) traits remains challenging due to their natural covariation. Using artificial seeds in enclosures, we quantified how these traits influence foraging decisions by Leopoldamys edwardsi, a dominant scatter-hoarding rodent in subtropical forests. Our results revealed a hierarchical order of trait importance: nutrient content > tannin content > coat thickness. High-nutrient seeds were preferentially consumed, while moderately nutrient-rich seeds (50% peanut powder) were most frequently scatter-hoarded, balancing immediate energy gain and long-term storage. Tannins exerted a dual effect: low concentrations (0.5%) enhanced consumption, likely due to reduced microbial decay, whereas high concentrations (7%) deterred both consumption and hoarding by impairing digestibility. Coat thickness had weaker effects but interacted with nutrients, as thin-coated, high-nutrient seeds were favored for both consumption and hoarding. Interactive effects highlighted a "benefit-first" decision framework, where rodents prioritize energy gain (nutrients), then modulate behavior to preserve benefits (tannins aiding storage), and finally account for handling costs (coat thickness). These findings illuminate coevolutionary dynamics between rodents and seeds, emphasizing how trait combinations shape mutualistic interactions critical for forest dynamics. Our study provides a mechanistic basis for predicting how shifts in seed traits may disrupt these interactions, with implications for ecosystem management.
(© 2026 International Society of Zoological Sciences, Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd.)
References: Barbehenn, R. V., and C. P. Constabel. 2011. “Tannins in Plant–Herbivore Interactions.” Phytochemistry 72: 1551–1565.
Bates, D., M. Machler, B. M. Bolker, and S. C. Walker. 2015. “Fitting Linear Mixed‐Effects Models Using lme4.” Journal of Statistical Software 67: 1–48.
Beckman, N. G., and L. L. Sullivan. 2023. “The Causes and Consequences of Seed Dispersal.” Annual Review of Ecology, Evolution, and Systematics 54: 403–427.
Bogdziewicz, M., D. Kelly, D. Ascoli, et al. 2024. “Evolutionary Ecology of Masting: Mechanisms, Models, and Climate Change.” Trends in Ecology & Evolution 39: 851–862.
Cao, L., Z. Wang, C. Yan, J. Chen, C. Guo, and Z. Zhang. 2016. “Differential Foraging Preferences on Seed Size by Rodents Result in Higher Dispersal Success of Medium‐Sized Seeds.” Ecology 97: 3070–3078.
Chang, G., Z. S. Xiao, and Z. B. Zhang. 2010. “Effects of Burrow Condition and Seed Handling Time on Hoarding Strategies of Edward's Long‐Tailed Rat (Leopoldamys edwardsi).” Behavioural Processes 85: 163–166.
Chang, G., and Z. Zhang. 2014. “Functional Traits Determine Formation of Mutualism and Predation Interactions in Seed‐Rodent Dispersal System of a Subtropical Forest.” Acta Oecologica 55: 43–50.
Cheng, J., H. He, L. Zheng, et al. 2024. “Bold Rats (Niviventer confucianus) Are More Effective in Seed Dispersal: Evidence Both Under Enclosure Conditions and in the Field.” Integrative Zoology 20: 740–754.
Dearing, M. D. 1997. “The Manipulation of Plant Toxins by a Food‐Hoarding Herbivore, Ochotona princeps.” Ecology 78: 774–781.
Dylewski, L., Y. K. Ortega, M. Bogdziewicz, and D. E. Pearson. 2020. “Seed Size Predicts Global Effects of Small Mammal Seed Predation on Plant Recruitment.” Ecology Letters 23: 1024–1033.
Feeny, P. 1970. “Seasonal Changes in Oak Leaf Tannins and Nutrients as a Cause of Spring Feeding by Winter Moth Caterpillars.” Ecology 51: 565–581.
Forget, P. M., J. E. Lambert, P. E. Hulme, and S. B. Vander Wall. 2005. Seed Fate: Predation, Dispersal and Seedling Establishment. CABI Publishing.
Fox, J., and S. Weisberg. 2019. An R Companion to Applied Regression., 3rd ed. Sage.
Hou, X., B. Zhang, M. A. Steele, et al. 2021. “Seed Traits and Rodent Community Interact to Determine Seed Fate: Evidence from Both Enclosure and Field Experiments.” Integrative Zoology 16: 939–954.
Jacobs, L. F. 1992. “The Effect of Handling Time on the Decision to Cache by Grey Squirrels.” Animal Behaviour 43: 522–524.
Karinho‐Betancourt, E., A. A. Agrawal, R. Halitschke, and J. Nunez‐Farfan. 2015. “Phylogenetic Correlations Among Chemical and Physical Plant Defenses Change with Ontogeny.” New Phytologist 206: 796–806.
Lai, J., Y. Zou, S. Zhang, X. Zhang, and L. Mao. 2022. “glmm.Hp: an R Package for Computing Individual Effect of Predictors in Generalized Linear Mixed Models.” Journal of Plant Ecology 15: 1302–1307.
Lai, Y., H. Dou, Y. Zhou, Z. Wang, L. Hou, and L. Cao. 2024. “Impact of Delayed Seed Drop on Rodent‐Mediated Seed Dispersal and Predation of Pine.” Integrative Zoology 20: 755–762.
Lenth, R. 2022. Emmeans: Estimated Marginal Means, aka Least‐Squares. https://cran.r-project.org/package=emmeans.
Lewis, A. R. 1982. “Selection of Nuts by Gray Squirrels and Optimal Foraging Theory.” American Midland Naturalist 107: 250–257.
Liu, H., J. Zhang, and B. Wang. 2023. “Contrasting Seed Traits of Co‐Existing Seeds Lead to a Complex Neighbor Effect in a Seed‐Rodent Interaction.” Oecologia 201: 1017–1024.
Nakagawa, S., and H. Schielzeth. 2013. “A General and Simple Method for Obtaining R2 from Generalized Linear Mixed‐Effects Models.” Methods in Ecology and Evolution 4: 133–142.
Niu, H., Z. Wang, G. Huang, C. Peng, Z. Zhang, and H. Zhang. 2020. “Responses of a Scatter‐Hoarding Squirrel to Conspecific Pilfering: A Test of the Reciprocal Pilferage Hypothesis.” Animal Behaviour 170: 147–155.
Paulsen, T. R., L. Colville, I. Kranner, et al. 2013. “Physical Dormancy in Seeds: A Game of Hide and Seek?” New Phytologist 198: 496–503.
Perea, R., A. San Miguel, and L. Gil. 2011. “Leftovers in Seed Dispersal: Ecological Implications of Partial Seed Consumption for Oak Regeneration.” Journal of Ecology 99: 194–201.
R Core Team. 2024. R: A Language and Environment for Statistical Computing. Version 4.4.0. R Foundation for Statistical Computing.
Renner, S. S., and C. M. Zohner. 2018. “Climate Change and Phenological Mismatch in Trophic Interactions Among Plants, Insects, and Vertebrates.” Annual Review of Ecology, Evolution, and Systematics 49: 165–182.
Saatkamp, A., A. Cochrane, L. Commander, et al. 2019. “A Research Agenda for Seed‐Trait Functional Ecology.” New Phytologist 221: 1764–1775.
Shimada, T., and T. Saitoh. 2006. “Re‐Evaluation of the Relationship Between Rodent Populations and Acorn Masting: A Review from the Aspect of Nutrients and Defensive Chemicals in Acorns.” Population Ecology 48: 341–352.
Stephens, R. B., E. A. Hobbie, T. D. Lee, and R. J. Rowe. 2019. “Pulsed Resource Availability Changes Dietary Niche Breadth and Partitioning Between Generalist Rodent Consumers.” Ecology and Evolution 9: 10681–10693.
Stone, L. 2020. “The Stability of Mutualism.” Nature Communications 11: 2648.
Sundaram, M., N. I. Lichti, N. J. O. Widmar, and R. K. Swihart. 2018. “Eastern Gray Squirrels Are Consistent Shoppers of Seed Traits: Insights from Discrete Choice Experiments.” Integrative Zoology 13: 280–296.
Sundaram, M., J. R. Willoughby, N. I. Lichti, M. A. Steele, and R. K. Swihart. 2015. “Segregating the Effects of Seed Traits and Common Ancestry of Hardwood Trees on Eastern Gray Squirrel Foraging Decisions.” PLoS ONE 10: e0130942.
Vander Wall, S. B. 2010. “How Plants Manipulate the Scatter‐Hoarding Behaviour of Seed‐Dispersing Animals.” Philosophical Transactions of the Royal Society B 365: 989–997.
Vander Wall, S. B., K. M. Kuhn, and M. J. Beck. 2005. “Seed Removal, Seed Predation, and Secondary Dispersal.” Ecology 86: 801–806.
Wang, B., and J. Chen. 2009. “Seed Size, More than Nutrient or Tannin Content, Affects Seed Caching Behavior of a Common Genus of Old World Rodents.” Ecology 90: 3023–3032.
Wang, B., J. S. Phillips, and K. W. Tomlinson. 2018. “Tradeoff Between Physical and Chemical Defense in Plant Seeds Is Mediated by Seed Mass.” Oikos 127: 440–447.
Wang, B., and X. Yang. 2015. “Seed Removal by Scatter‐Hoarding Rodents: The Effects of Tannin and Nutrient Concentration.” Behavioural Processes 113: 94–98.
Wang, M., X. Yang, and X. Yi. 2023. “Effects of Seed Traits on the Cache Size of a Scatter‐Hoarding Rodent, Leopoldamys edwardsi.” Behavioral Ecology and Sociobiology 77: 105.
Wang, M., and X. Yi. 2022. “The Effects of Seed Detectability and Seed Traits on Hoarding Preference of Two Rodent Species.” Integrative Zoology 17: 944–952.
Wang, Z., Y. Zhang, D. Zhang, J. Li, and X. Yi. 2016. “Nutritional and Defensive Properties of Fagaceae Nuts Dispersed by Animals: A Multiple Species Study.” European Journal of Forest Research 135: 911–917.
Xiao, Z., X. Gao, and Z. Zhang. 2013. “Sensitivity to Seed Germination Schedule by Scatter‐Hoarding Pére David's Rock Squirrels During Mast and Non‐Mast Years.” Ethology 119: 472–479.
Xiao, Z., M. Holyoak, C. J. Krebs, and X. Huang. 2022. “Palatability and Profitability of Co‐Occurring Seeds Alter Indirect Interactions Among Rodent‐Dispersed Trees.” Integrative Zoology 17: 206–216.
Xiao, Z., Y. Wang, M. Harris, and Z. Zhang. 2006. “Spatial and Temporal Variation of Seed Predation and Removal of Sympatric Large‐Seeded Species in Relation to Innate Seed Traits in a Subtropical Forest, Southwest China.” Forest Ecology and Management 222: 46–54.
Yadok, B. G., P.‐M. Forget, D. Gerhard, B. Aliyu, and H. Chapman. 2020. “Seed Nutrient Content Rather Than Size Influences Seed Dispersal by Scatterhoarding Rodents in a West African Montane Forest.” Journal of Tropical Ecology 36: 174–181.
Yang, X., L. Han, Y. Wang, C. Guo, and Z. Zhang. 2022. “Revealing the Real‐Time Diversity and Abundance of Small Mammals by Using an Intelligent Animal Monitoring System (IAMS).” Integrative Zoology 17: 1121–1135.
Yang, X., C. Yan, H. Gu, and Z. Zhang. 2020. “Interspecific Synchrony of Seed Rain Shapes Rodent‐Mediated Indirect Seed‐Seed Interactions of Sympatric Tree Species in a Subtropical Forest.” Ecology Letters 23: 45–54.
Yang, X., C. Yan, Q. Zhao, et al. 2018. “Ecological Succession Drives the Structural Change of Seed‐Rodent Interaction Networks in Fragmented Forests.” Forest Ecology and Management 419–420: 42–50.
Yang, X., K. Zhao, F. Ma, et al. 2025a. “Dissecting the Roles of Seed Nutrient Content and Coat Thickness in Seed Dispersal and Fate Mediated by Rodents: A Field Experiment Using Artificial Seeds.” Forest Ecology and Management 585: 122650.
Yang, X., K. Zhao, C. Yan, B. Wang, and Z. Zhang. 2023. “Impacts of Moderateness and Cobalancedness in Seed Mass and Coat Thickness on Seed Dispersal Effectiveness of Quercus variabilis by Rodents.” Plant Ecology 224: 283–297.
Yang, X., K. Zhao, and Z. Zhang. 2025b. “Environmental Gradients Drive Context‐Dependent Seed Fate: Synergistic Roles of Forest Succession, Edge Effects, and Masting in Shaping Rodent Dispersal Dynamics.” Biological Conservation 312: 111478.
Yu, F., L. Zhang, Y. Wang, et al. 2023. “High Rodent Abundance Increases Seed Removal but Decreases Scatter‐Hoarding and Seedling Recruitment Along an Elevational Gradient.” Integrative Zoology 18: 843–858.
Yu, F., M. Zhang, Y. Yang, Y. Wang, and X. Yi. 2025. “Seed Size and Dispersal Mode Select Mast Seeding in Perennial Plants.” Integrative Zoology 20: 171–185.
Zhang, H., J. Cheng, Z. Xiao, and Z. Zhang. 2008. “Effects of Seed Abundance on Seed Scatter‐Hoarding of Edward's Rat (Leopoldamys edwardsi Muridae) at the Individual Level.” Oecologia 158: 57–63.
Zhang, H., and Z. Zhang. 2008. “Endocarp Thickness Affects Seed Removal Speed by Small Rodents in a Warm‐Temperate Broad‐Leafed Deciduous Forest, China.” Acta Oecologica 34: 285–293.
Zhang, M., M. A. Steele, and X. Yi. 2013. “Reconsidering the Effects of Tannin on Seed Dispersal by Rodents: Evidence from Enclosure and Field Experiments with Artificial Seeds.” Behavioural Processes 100: 200–207.
Zhang, Z., Z. Wang, G. Chang, et al. 2016. “Trade‐Off Between Seed Defensive Traits and Impacts on Interaction Patterns Between Seeds and Rodents in Forest Ecosystems.” Plant Ecology 217: 253–265.
Zhao, X., J. Guo, Y. Wang, and X. Yi. 2024. “High‐Tannin Food Enhances Spatial Memory and Scatter‐Hoarding in Rodents via the Microbiota‐Gut‐Brain Axis.” Microbiome 12: 140.
Zhu, Y., X. Yang, H. Gu, Y. Teng, and Z. Zhang. 2021. “Effects of Seed Coat Thickness on Rodents' Seed Dispersal Behavior and Seed Fate.” Acta Theriologica Sinica 41: 667–675.
Zwolak, R., P. Celebias, and M. Bogdziewicz. 2022. “Global Patterns in the Predator Satiation Effect of Masting: A Meta‐Analysis.” Proceedings of the National Academy of Sciences of the United States of America 119: e2105655119.
Grant Information: 32371593 National Natural Science Foundation of China; 32001123 National Natural Science Foundation of China; 2024NSFSC2080 Science and Technology‒Education Joint Foundation of Sichuan Province; 24KE039 Fundamental Research Funds of China West Normal University; S202410638108 Undergraduate Innovation and Entrepreneurship Training Program of China West Normal University; cxcy2024284 Undergraduate Innovation and Entrepreneurship Training Program of China West Normal University; the Youth Project of the Tianfu Emei Plan in Sichuan Province
Contributed Indexing: Keywords: Leopoldamys edwardsi; artificial seeds; scatter‐hoarding; seed dispersal; seed predation; seed traits
Substance Nomenclature: 0 (Tannins)
Entry Date(s): Date Created: 20260213 Date Completed: 20260714 Latest Revision: 20260726
Update Code: 20260726
PubMed Central ID: PMC13362269
DOI: 10.1111/1749-4877.70067
PMID: 41684159
Βάση Δεδομένων: MEDLINE
Περιγραφή
ISSN:1749-4877
DOI:10.1111/1749-4877.70067